Urban coyotes are genetically distinct from coyotes in natural habitats

Urbanization is increasing throughout the world, transforming natural habitats. Coyotes (Canis latrans) are found in highly urban, suburban, rural and undeveloped mountainous habitats, making them an exemplary model organism to investigate the effects of urbanization on animals. We hypothesized that coyotes in natural habitats are more genetically related to distant coyotes in similar natural habitats and less related to coyotes in urban areas due to natal habitat-biased dispersal. We also hypothesized that increasing urbanization would result in decreased genetic diversity due to habitat fragmentation, dispersal barriers and genetic drift. We analyzed 10 microsatellite genetic markers from 125 individual coyotes sampled across a spectrum of highly urban to highly natural areas in southern California. Most coyotes clustered into four distinct genetic populations, whereas others appeared to have admixed ancestry. Three genetic populations were associated primarily with urban habitats in Los Angeles and Orange Counties. In contrast, the remaining population was associated with more naturally vegetated land near the surrounding mountains. Coyotes living in natural areas formed a genetically distinct cluster despite long geographic distances separating them. Genetic diversity was negatively associated with urban/suburban land cover and local road density, and positively associated with the relative amount of natural vegetation. These results indicate that genetic differentiation and loss of genetic diversity coincided with the extremely rapid expansion of Greater Los Angeles throughout the 1900s. Thus, urbanization reduces gene flow and erodes genetic diversity even in a habitat generalist thought to be minimally impacted by land development.

[1]  Justin L. Brown,et al.  Effects of urbanization on resource use and individual specialization in coyotes (Canis latrans) in southern California , 2020, PloS one.

[2]  Claudia Wultsch,et al.  Genetic diversity and relatedness of a recently established population of eastern coyotes (Canis latrans) in New York City , 2019, Urban Ecosystems.

[3]  Lindsay S. Miles,et al.  Gene flow and genetic drift in urban environments , 2019, Molecular ecology.

[4]  Jacqueline L. Frair,et al.  Spatial genetic analysis of coyotes in New York State , 2019, Wildlife Society Bulletin.

[5]  K. Miller,et al.  Geographic patterns in morphometric and genetic variation for coyote populations with emphasis on southeastern coyotes , 2019, Ecology and evolution.

[6]  P. Mahoney,et al.  The intrepid urban coyote: a comparison of bold and exploratory behavior in coyotes from urban and rural environments , 2019, Scientific Reports.

[7]  J. Fitzsimons,et al.  Bringing the city to the country: relationships between streetscape vegetation type and bird assemblages in a major regional centre , 2019, Journal of Urban Ecology.

[8]  B. vonHoldt,et al.  Genetics of urban colonization: neutral and adaptive variation in coyotes (Canis latrans) inhabiting the New York metropolitan area , 2019, Journal of Urban Ecology.

[9]  M. Fortin,et al.  A roadmap for urban evolutionary ecology , 2018, Evolutionary applications.

[10]  J. Mateo,et al.  Parental habituation to human disturbance over time reduces fear of humans in coyote offspring , 2018, Ecology and evolution.

[11]  H. Sand,et al.  No place like home? A test of the natal habitat-biased dispersal hypothesis in Scandinavian wolves , 2018, Royal Society Open Science.

[12]  D. Schluter,et al.  Speciation and the City. , 2018, Trends in ecology & evolution.

[13]  Lindsay S. Miles,et al.  Urban hubs of connectivity: contrasting patterns of gene flow within and among cities in the western black widow spider , 2018, Proceedings of the Royal Society B: Biological Sciences.

[14]  Bruno M. Ghersi,et al.  Urban rat races: spatial population genomics of brown rats (Rattus norvegicus) compared across multiple cities , 2018, Proceedings of the Royal Society B: Biological Sciences.

[15]  Christopher J. Schell Urban Evolutionary Ecology and the Potential Benefits of Implementing Genomics , 2018, The Journal of heredity.

[16]  R. Wayne,et al.  Determining the drivers of population structure in a highly urbanized landscape to inform conservation planning , 2018, Conservation biology : the journal of the Society for Conservation Biology.

[17]  Susanne A. Fritz,et al.  Moving in the Anthropocene: Global reductions in terrestrial mammalian movements , 2018, Science.

[18]  Emily E. Puckett,et al.  Spatial population genomics of the brown rat (Rattus norvegicus) in New York City , 2018, Molecular ecology.

[19]  A. Charmantier,et al.  Great tits and the city: Distribution of genomic diversity and gene–environment associations along an urbanization gradient , 2017, Evolutionary applications.

[20]  Marc T. J. Johnson,et al.  Evolution of life in urban environments , 2017, Science.

[21]  M. Alberti,et al.  Urban driven phenotypic changes: empirical observations and theoretical implications for eco-evolutionary feedback , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[22]  N. Duncan,et al.  Initial colonization of Long Island, New York by the eastern coyote, Canis latrans (Carnivora, Canidae), including first record of breeding , 2017 .

[23]  H. Ernest,et al.  Interactions between demography, genetics, and landscape connectivity increase extinction probability for a small population of large carnivores in a major metropolitan area , 2016, Proceedings of the Royal Society B: Biological Sciences.

[24]  M. Veith,et al.  Cityscape genetics: structural vs. functional connectivity of an urban lizard population , 2016, Molecular ecology.

[25]  R. Sikes,et al.  2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education , 2016, Journal of Mammalogy.

[26]  Aaron M. Haines,et al.  Genetic differences in the response to landscape fragmentation by a habitat generalist, the bobcat, and a habitat specialist, the ocelot , 2016, Conservation Genetics.

[27]  J. Munshi‐South,et al.  Population genomics of the Anthropocene: urbanization is negatively associated with genome‐wide variation in white‐footed mouse populations , 2016, Evolutionary applications.

[28]  R. Bivand,et al.  Tools for Reading and Handling Spatial Objects , 2016 .

[29]  C. Donihue,et al.  Adaptive evolution in urban ecosystems , 2015, AMBIO.

[30]  A. Piaggio,et al.  Assessment of Population Structure of Coyotes in East-Central Alabama using Microsatellite DNA , 2015 .

[31]  R. Wayne,et al.  Disease and freeways drive genetic change in urban bobcat populations , 2014, Evolutionary applications.

[32]  H. Ernest,et al.  Individual Behaviors Dominate the Dynamics of an Urban Mountain Lion Population Isolated by Roads , 2014, Current Biology.

[33]  J. Monzón First regional evaluation of nuclear genetic diversity and population structure in northeastern coyotes ( Canis latrans) , 2014, F1000Research.

[34]  J. Janecka,et al.  Loss of Genetic Diversity among Ocelots in the United States during the 20th Century Linked to Human Induced Population Reductions , 2014, PloS one.

[35]  R. Kays,et al.  Assessment of coyote–wolf–dog admixture using ancestry‐informative diagnostic SNPs , 2014, Molecular ecology.

[36]  H. Schielzeth,et al.  Urbanization and its effects on personality traits: a result of microevolution or phenotypic plasticity? , 2013, Global change biology.

[37]  J. Monzón Rapid Evolution of Northeastern Coyotes , 2012 .

[38]  B. vonHoldt,et al.  STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method , 2012, Conservation Genetics Resources.

[39]  S. Magle,et al.  Urban wildlife research: Past, present, and future , 2012 .

[40]  Rod Peakall,et al.  GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update , 2012, Bioinform..

[41]  S. Gehrt,et al.  Long-term pair bonding and genetic evidence for monogamy among urban coyotes (Canis latrans) , 2012 .

[42]  J. Chadwick,et al.  Red wolf natal dispersal characteristics: comparing periods of population increase and stability , 2012 .

[43]  Robert N. Fisher,et al.  A Rapid, Strong, and Convergent Genetic Response to Urban Habitat Fragmentation in Four Divergent and Widespread Vertebrates , 2010, PloS one.

[44]  J. Munshi‐South,et al.  Rapid, pervasive genetic differentiation of urban white‐footed mouse (Peromyscus leucopus) populations in New York City , 2010, Molecular ecology.

[45]  E C Anderson,et al.  The influence of family groups on inferences made with the program Structure , 2008, Molecular ecology resources.

[46]  Noah A. Rosenberg,et al.  ADZE: a rarefaction approach for counting alleles private to combinations of populations , 2008, Bioinform..

[47]  R. A. Krebs,et al.  Population Structure of Coyote (Canis latrans) in the Urban Landscape of the Cleveland, Ohio Area , 2008 .

[48]  H. Ernest,et al.  Coyotes demonstrate how habitat specialization by individuals of a generalist species can diversify populations in a heterogeneous ecoregion. , 2008, Molecular biology and evolution.

[49]  Noah A. Rosenberg,et al.  CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure , 2007, Bioinform..

[50]  R. Wayne,et al.  FAST‐TRACK: A southern California freeway is a physical and social barrier to gene flow in carnivores , 2006, Molecular ecology.

[51]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[52]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[53]  H. Ernest,et al.  Coyote movements and social structure along a cryptic population genetic subdivision , 2005, Molecular ecology.

[54]  L. Kruuk,et al.  Evolution driven by differential dispersal within a wild bird population , 2005, Nature.

[55]  J. Stamps,et al.  The effect of natal experience on habitat preferences. , 2004, Trends in ecology & evolution.

[56]  H. Ernest,et al.  Population structure of California coyotes corresponds to habitat‐specific breaks and illuminates species history , 2004, Molecular ecology.

[57]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. , 2003, Genetics.

[58]  R. Wayne,et al.  Effects of Urbanization and Habitat Fragmentation on Bobcats and Coyotes in Southern California , 2003 .

[59]  Louie H. Yang,et al.  The Ecology of Individuals: Incidence and Implications of Individual Specialization , 2002, The American Naturalist.

[60]  F. Galibert,et al.  Chromosome-specific single-locus FISH probes allow anchorage of an 1800-marker integrated radiation-hybrid/linkage map of the domestic dog genome to all chromosomes. , 2001, Genome research.

[61]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[62]  M. Lynch,et al.  Estimation of pairwise relatedness with molecular markers. , 1999, Genetics.

[63]  E. Ostrander,et al.  A linkage map of the canine genome. , 1997, Genomics.

[64]  E. Ostrander,et al.  A class of highly polymorphic tetranucleotide repeats for canine genetic mapping , 1996, Mammalian Genome.

[65]  E. Ostrander,et al.  Patterns of differentiation and hybridization in North American wolflike canids, revealed by analysis of microsatellite loci. , 1994, Molecular biology and evolution.

[66]  J. Rine,et al.  Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. , 1993, Genomics.

[67]  N. Lehman,et al.  Analysis of coyote mitochondrial DNA genotype frequencies: estimation of the effective number of alleles. , 1991, Genetics.

[68]  K. Immelmann Ecological Significance of Imprinting and Early Learning , 1975 .

[69]  H. B. Kettlewell,et al.  Selection experiments on industrial melanism in the Lepidoptera , 1955, Heredity.

[70]  S. Riley,et al.  Infectious Disease and Contaminants in Urban Wildlife: Unseen and Often Overlooked Threats , 2014 .

[71]  Theunis Piersma,et al.  The interplay between habitat availability and population differentiation , 2012 .

[72]  Kelli L. Larson,et al.  A Multi-Scalar Approach to Theorizing Socio-Ecological Dynamics of Urban Residential Landscapes , 2011 .

[73]  Justin L. Brown,et al.  Is the Urban Coyote a Misanthropic Synanthrope? The C ase from Chicago , 2011 .